Interplay between Feedback and Feedforward Control in Fly Gaze Stabilization

Abstract Flies rely on a powerful gaze stabilization reflex to facilitate visual control and guidance of flight. We performed behavioral experiments and systems identification to study the contribution of two major sensory systems to gaze stabilization: the mechanosensory halteres, and the compound eyes. We measured the frequency response of compensatory head roll induced by forced thorax movements with and without halteres. Based on a simplified, linear architecture, we derived transfer functions for the two sensory pathways and the neck motor system that actuates changes of head position. The resulting bandwidths and response delays were consistent with data from the literature.

[1]  R. Hengstenberg.  Multisensory control in insect oculomotor systems. , 1993, Reviews of oculomotor research.

[2]  R. Hengstenberg,et al.  Compensatory head roll in the blowfly Calliphora during flight , 1986, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[3]  C. Gilbert,et al.  Oculomotor control in calliphorid flies: Head movements during activation and inhibition of neck motor neurons corroborate neuroanatomical predictions , 1995, The Journal of comparative neurology.

[4]  Mark A Frye,et al.  Multisensory systems integration for high-performance motor control in flies , 2010, Current Opinion in Neurobiology.

[5]  Roland Hengstenberg,et al.  Gaze control in the blowfly Calliphora: a multisensory, two-stage integration process , 1991 .

[6]  Rik Pintelon,et al.  System Identification: A Frequency Domain Approach , 2012 .

[7]  H. Markl,et al.  Head Movements in Flies ( Calliphora ) Produced by Deflexion of the Halteres , 1980 .

[8]  G. Nalbach,et al.  Extremely non-orthogonal axes in a sense organ for rotation: Behavioural analysis of the dipteran haltere system , 1994, Neuroscience.

[9]  Holger G Krapp,et al.  Nonlinear Integration of Visual and Haltere Inputs in Fly Neck Motor Neurons , 2009, The Journal of Neuroscience.

[10]  M. Srinivasan,et al.  Visual regulation of ground speed and headwind compensation in freely flying honey bees (Apis mellifera L.) , 2006, Journal of Experimental Biology.

[11]  K. Kawachi,et al.  Response characteristics of visual altitude control system in Bombus terrestris , 2006, Journal of Experimental Biology.

[12]  H. Krapp,et al.  Sensory Systems and Flight Stability: What do Insects Measure and Why? , 2007 .

[13]  N. Strausfeld,et al.  The neck motor system of the fly Calliphora erythrocephala. I: Muscles and motor neurons , 1987 .

[14]  Hateren,et al.  Blowfly flight and optic flow. II. Head movements during flight , 1999, The Journal of experimental biology.

[15]  M. Araki,et al.  Two-Degree-of-Freedom PID Controllers , 2003 .

[16]  Steven N Fry,et al.  Frequency response of lift control in Drosophila , 2010, Journal of The Royal Society Interface.